Aging distorts the representation of emotions by amplifying prefrontal variability

Abstract

Understanding the mechanisms behind the variability of neural signals holds the key to the characterization of developmental and lifespan aging trajectories. Here we propose that tracking temporally structured neural fluctuations or volatility in brain areas during naturalistic tasks provides a more salient characterization of ageing trajectories compared to measures based on mean and resting-state variability. Compared to other prefrontal regions, the orbitofrontal cortices (OFC) exhibit higher BOLD signal variability in aged individuals. Neural latent state analysis revealed that, in contrast to the stable representations in younger adults, the OFC in older adults exhibited more temporally distorted representations, mirroring their distinct affective experiences. Furthermore, lower OFC volatility during the movie was associated with participants bias toward positive responses in a separate emotional reactivity task. This suggests orbitofrontal neural volatility might be a general adaptive response to affective computations. To investigate this further, a Bayesian learning model of valence dynamics was employed, which revealed that older adults exhibit heightened uncertainty in neural representations while estimating affective states. Collectively, these results indicate that neural volatility identified through BOLD variability carries unique information about older adults affective experiences and how naturalistic neuroimaging can chart a way forward in understanding this better.